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Intrinsic coupling modes reveal the functional architecture of cortico-tectal networks.

Stitt I, Galindo-Leon E, Pieper F, Engler G, Fiedler E, Stieglitz T, Engel AK - Sci Adv (2015)

Bottom Line: We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales.Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity.Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.

ABSTRACT
In the absence of sensory stimulation or motor output, the brain exhibits complex spatiotemporal patterns of intrinsically generated neural activity. Analysis of ongoing brain dynamics has identified the prevailing modes of cortico-cortical interaction; however, little is known about how such patterns of intrinsically generated activity are correlated between cortical and subcortical brain areas. We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales. Ongoing cortico-tectal interaction was characterized by correlated fluctuations in the amplitude of delta, spindle, low gamma, and high-frequency oscillations (>100 Hz). Of these identified coupling modes, topographical patterns of high-frequency coupling were the most consistent with patterns of anatomical connectivity, reflecting synchronized spiking within cortico-tectal networks. Cortico-tectal coupling at high frequencies was temporally parcellated by the phase of slow cortical oscillations and was strongest for SC-cortex channel pairs that displayed overlapping visual spatial receptive fields. Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity. Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

No MeSH data available.


Related in: MedlinePlus

Dynamics and large-scale topography of cortico-cortical and cortico-tectal amplitude envelope correlation.(A) Top: Population-averaged amplitude envelope correlation computed between μECoG contact pairs separated by varying distances. Note that correlations are widely distributed in slow (~0.7 Hz), delta (~3 Hz), and spindle (8 to 15 Hz) frequency ranges and that amplitude envelopes are minimally correlated for frequencies above 120 Hz. Middle: Population-averaged amplitude envelope correlation computed between intracortical and μECoG recording sites. Bottom: Population-averaged cortico-tectal amplitude envelope correlation computed for SC recording contacts located in superficial (blue) and deep (red) SC layers. Note the peaks in cortico-tectal amplitude correlation for delta, spindle, and gamma frequencies. (B) Average cortical topography of cortico-tectal amplitude correlation for delta, spindle, and gamma (30 to 45 Hz) carrier frequencies. Maps are plotted for both superficial and deep SC layers. To compare functional coupling to anatomy, we plotted the density of tectally projecting neurons across the cortical surface. Anatomical data were adapted with permission from Fig. 1 in (13). (C) Spatial correlation of anatomical connectivity (B, bottom) and functional coupling topographies across all frequencies. The z score of correlation coefficients was estimated by computing the spatial correlation of randomly scrambled amplitude correlation topographies and anatomical data. Analyses for superficial and deep layers are plotted in blue and red, respectively.
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Figure 2: Dynamics and large-scale topography of cortico-cortical and cortico-tectal amplitude envelope correlation.(A) Top: Population-averaged amplitude envelope correlation computed between μECoG contact pairs separated by varying distances. Note that correlations are widely distributed in slow (~0.7 Hz), delta (~3 Hz), and spindle (8 to 15 Hz) frequency ranges and that amplitude envelopes are minimally correlated for frequencies above 120 Hz. Middle: Population-averaged amplitude envelope correlation computed between intracortical and μECoG recording sites. Bottom: Population-averaged cortico-tectal amplitude envelope correlation computed for SC recording contacts located in superficial (blue) and deep (red) SC layers. Note the peaks in cortico-tectal amplitude correlation for delta, spindle, and gamma frequencies. (B) Average cortical topography of cortico-tectal amplitude correlation for delta, spindle, and gamma (30 to 45 Hz) carrier frequencies. Maps are plotted for both superficial and deep SC layers. To compare functional coupling to anatomy, we plotted the density of tectally projecting neurons across the cortical surface. Anatomical data were adapted with permission from Fig. 1 in (13). (C) Spatial correlation of anatomical connectivity (B, bottom) and functional coupling topographies across all frequencies. The z score of correlation coefficients was estimated by computing the spatial correlation of randomly scrambled amplitude correlation topographies and anatomical data. Analyses for superficial and deep layers are plotted in blue and red, respectively.

Mentions: Before assessing the dynamics of simultaneously recorded SC and cortical activity, we first wanted to identify the spectral signatures that define cortico-cortical functional connectivity under isoflurane anesthesia (for average ongoing power spectra of SC, intracortical, and μECoG recording sites, see fig. S1). To this end, we computed the correlation of band-limited signal amplitudes between all possible combinations of μECoG recording contacts. Figure 2A illustrates the strength of amplitude correlation for each carrier frequency as a function of μECoG inter-electrode distance. Amplitude envelopes of oscillations in the slow (~0.7 Hz), delta (~3 Hz), and spindle (~11 Hz) frequencies were correlated over large distances in the cortex. For frequencies above 30 Hz, amplitude envelope correlation gradually decreased with increasing frequency such that μECoG signal frequencies above 120 Hz displayed minimal inter-electrode amplitude envelope correlation, suggesting that such high-frequency μECoG signal components reflect neural activity at a more local scale. To validate the cortico-cortical functional connectivity findings from μECoG LFPs, we repeated the same amplitude envelope correlation analysis between intracortical recording sites and μECoG contacts (Fig. 2A). Indeed, intracortical-μECoG amplitude envelope correlation displayed the same spectral characteristics, with spontaneous amplitude fluctuations strongly correlated for slow (~0.7 Hz), delta (~3 Hz), and spindle (~11 Hz) frequencies over larger distances.


Intrinsic coupling modes reveal the functional architecture of cortico-tectal networks.

Stitt I, Galindo-Leon E, Pieper F, Engler G, Fiedler E, Stieglitz T, Engel AK - Sci Adv (2015)

Dynamics and large-scale topography of cortico-cortical and cortico-tectal amplitude envelope correlation.(A) Top: Population-averaged amplitude envelope correlation computed between μECoG contact pairs separated by varying distances. Note that correlations are widely distributed in slow (~0.7 Hz), delta (~3 Hz), and spindle (8 to 15 Hz) frequency ranges and that amplitude envelopes are minimally correlated for frequencies above 120 Hz. Middle: Population-averaged amplitude envelope correlation computed between intracortical and μECoG recording sites. Bottom: Population-averaged cortico-tectal amplitude envelope correlation computed for SC recording contacts located in superficial (blue) and deep (red) SC layers. Note the peaks in cortico-tectal amplitude correlation for delta, spindle, and gamma frequencies. (B) Average cortical topography of cortico-tectal amplitude correlation for delta, spindle, and gamma (30 to 45 Hz) carrier frequencies. Maps are plotted for both superficial and deep SC layers. To compare functional coupling to anatomy, we plotted the density of tectally projecting neurons across the cortical surface. Anatomical data were adapted with permission from Fig. 1 in (13). (C) Spatial correlation of anatomical connectivity (B, bottom) and functional coupling topographies across all frequencies. The z score of correlation coefficients was estimated by computing the spatial correlation of randomly scrambled amplitude correlation topographies and anatomical data. Analyses for superficial and deep layers are plotted in blue and red, respectively.
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Related In: Results  -  Collection

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Figure 2: Dynamics and large-scale topography of cortico-cortical and cortico-tectal amplitude envelope correlation.(A) Top: Population-averaged amplitude envelope correlation computed between μECoG contact pairs separated by varying distances. Note that correlations are widely distributed in slow (~0.7 Hz), delta (~3 Hz), and spindle (8 to 15 Hz) frequency ranges and that amplitude envelopes are minimally correlated for frequencies above 120 Hz. Middle: Population-averaged amplitude envelope correlation computed between intracortical and μECoG recording sites. Bottom: Population-averaged cortico-tectal amplitude envelope correlation computed for SC recording contacts located in superficial (blue) and deep (red) SC layers. Note the peaks in cortico-tectal amplitude correlation for delta, spindle, and gamma frequencies. (B) Average cortical topography of cortico-tectal amplitude correlation for delta, spindle, and gamma (30 to 45 Hz) carrier frequencies. Maps are plotted for both superficial and deep SC layers. To compare functional coupling to anatomy, we plotted the density of tectally projecting neurons across the cortical surface. Anatomical data were adapted with permission from Fig. 1 in (13). (C) Spatial correlation of anatomical connectivity (B, bottom) and functional coupling topographies across all frequencies. The z score of correlation coefficients was estimated by computing the spatial correlation of randomly scrambled amplitude correlation topographies and anatomical data. Analyses for superficial and deep layers are plotted in blue and red, respectively.
Mentions: Before assessing the dynamics of simultaneously recorded SC and cortical activity, we first wanted to identify the spectral signatures that define cortico-cortical functional connectivity under isoflurane anesthesia (for average ongoing power spectra of SC, intracortical, and μECoG recording sites, see fig. S1). To this end, we computed the correlation of band-limited signal amplitudes between all possible combinations of μECoG recording contacts. Figure 2A illustrates the strength of amplitude correlation for each carrier frequency as a function of μECoG inter-electrode distance. Amplitude envelopes of oscillations in the slow (~0.7 Hz), delta (~3 Hz), and spindle (~11 Hz) frequencies were correlated over large distances in the cortex. For frequencies above 30 Hz, amplitude envelope correlation gradually decreased with increasing frequency such that μECoG signal frequencies above 120 Hz displayed minimal inter-electrode amplitude envelope correlation, suggesting that such high-frequency μECoG signal components reflect neural activity at a more local scale. To validate the cortico-cortical functional connectivity findings from μECoG LFPs, we repeated the same amplitude envelope correlation analysis between intracortical recording sites and μECoG contacts (Fig. 2A). Indeed, intracortical-μECoG amplitude envelope correlation displayed the same spectral characteristics, with spontaneous amplitude fluctuations strongly correlated for slow (~0.7 Hz), delta (~3 Hz), and spindle (~11 Hz) frequencies over larger distances.

Bottom Line: We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales.Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity.Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany.

ABSTRACT
In the absence of sensory stimulation or motor output, the brain exhibits complex spatiotemporal patterns of intrinsically generated neural activity. Analysis of ongoing brain dynamics has identified the prevailing modes of cortico-cortical interaction; however, little is known about how such patterns of intrinsically generated activity are correlated between cortical and subcortical brain areas. We investigate the correlation structure of ongoing cortical and superior colliculus (SC) activity across multiple spatial and temporal scales. Ongoing cortico-tectal interaction was characterized by correlated fluctuations in the amplitude of delta, spindle, low gamma, and high-frequency oscillations (>100 Hz). Of these identified coupling modes, topographical patterns of high-frequency coupling were the most consistent with patterns of anatomical connectivity, reflecting synchronized spiking within cortico-tectal networks. Cortico-tectal coupling at high frequencies was temporally parcellated by the phase of slow cortical oscillations and was strongest for SC-cortex channel pairs that displayed overlapping visual spatial receptive fields. Despite displaying a high degree of spatial specificity, cortico-tectal coupling in lower-frequency bands did not match patterns of cortex-to-SC anatomical connectivity. Collectively, our findings demonstrate that neural activity is spontaneously coupled between cortex and SC, with high- and low-frequency modes of coupling reflecting direct and indirect cortico-tectal interactions, respectively.

No MeSH data available.


Related in: MedlinePlus